Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia

Significance

In 2016/2017, highly pathogenic avian influenza (HPAI) virus of the subtype H5 spilled over into wild birds and caused the largest known HPAI epidemic in Europe, affecting poultry and wild birds. During its spread, the virus frequently exchanged genetic material (reassortment) with cocirculating low-pathogenic avian influenza viruses. To determine where and when these reassortments occurred, we analyzed Eurasian avian influenza viruses and identified a large set of H5 HPAI reassortants. We found that new genetic material likely came from wild birds across their migratory range and from domestic ducks not only in China, but also in central Europe. This knowledge is important to understand how the virus could adapt to wild birds and become established in wild bird populations.

Abstract

Highly pathogenic avian influenza (HPAI) viruses of the H5 A/goose/Guangdong/1/96 lineage can cause severe disease in poultry and wild birds, and occasionally in humans. In recent years, H5 HPAI viruses of this lineage infecting poultry in Asia have spilled over into wild birds and spread via bird migration to countries in Europe, Africa, and North America. In 2016/2017, this spillover resulted in the largest HPAI epidemic on record in Europe and was associated with an unusually high frequency of reassortments between H5 HPAI viruses and cocirculating low-pathogenic avian influenza viruses. Here, we show that the seven main H5 reassortant viruses had various combinations of gene segments 1, 2, 3, 5, and 6. Using detailed time-resolved phylogenetic analysis, most of these gene segments likely originated from wild birds and at dates and locations that corresponded to their hosts’ migratory cycles. However, some gene segments in two reassortant viruses likely originated from domestic anseriforms, either in spring 2016 in east China or in autumn 2016 in central Europe. Our results demonstrate that, in addition to domestic anseriforms in Asia, both migratory wild birds and domestic anseriforms in Europe are relevant sources of gene segments for recent reassortant H5 HPAI viruses. The ease with which these H5 HPAI viruses reassort, in combination with repeated spillovers of H5 HPAI viruses into wild birds, increases the risk of emergence of a reassortant virus that persists in wild bird populations yet remains highly pathogenic for poultry.